Maternal immune activation induces GAD1 and GAD2 promoter remodeling in the offspring prefrontal cortex

References

• Brown AS, Derkits EJ. Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am J Psychiatry 2010; 167:261–80; PMID:20123911; http://dx.doi.org/10.1176/appi.ajp.2009.09030361
   PubMed Web of Science ®Google Scholar
• Canetta S, Sourander A, Surcel HM, Hinkka-Yli-Salomäki S, Leiviskä J, Kellendonk C, McKeague IW, Brown AS. Elevated maternal C-reactive protein and increased risk of schizophrenia in a national birth cohort. Am J Psychiatry 2014; 171:960–8; PMID:24969261; http://dx.doi.org/10.1176/appi.ajp.2014.13121579
   PubMed Web of Science ®Google Scholar
• Atladóttir HO, Thorsen P, Østergaard L, Schendel DE, Lemcke S, Abdallah M, Parner ET. Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J Autism Dev Disord 2010; 40:1423–30; http://dx.doi.org/10.1007/s10803-010-1006-y
   PubMed Web of Science ®Google Scholar
• Brown AS, Sourander A, Hinkka-Yli-Salomäki S, McKeague IW, Sundvall J, Surcel HM. Elevated maternal C-reactive protein and autism in a national birth cohort. Mol Psychiatry 2014; 19:259–64; PMID:23337946; http://dx.doi.org/10.1038/mp.2012.197
   PubMed Web of Science ®Google Scholar
• Parboosing R, Bao Y, Shen L, Schaefer CA, Brown AS. Gestational influenza and bipolar disorder in adult offspring. JAMA Psychiatry 2013; 70:677–85; PMID:23699867; http://dx.doi.org/10.1001/jamapsychiatry.2013.896
   PubMed Web of Science ®Google Scholar
• Canetta SE, Bao Y, Co MD, Ennis FA, Cruz J, Terajima M, Shen L, Kellendonk C, Schaefer CA, Brown AS. Serological documentation of maternal influenza exposure and bipolar disorder in adult offspring. Am J Psychiatry 2014; 171:557–63; PMID:24480930; http://dx.doi.org/10.1176/appi.ajp.2013.13070943
   PubMed Web of Science ®Google Scholar
• Harvey L, Boksa P. Prenatal and postnatal animal models of immune activation: relevance to a range of neurodevelopmental disorders. Dev Neurobiol 2012; 72:1335–48; PMID:22730147; http://dx.doi.org/10.1002/dneu.22043
   PubMed Web of Science ®Google Scholar
• Meyer U. Prenatal poly(I:C) exposure and other developmental immune activation models in rodent systems. Biol Psychiatry 2014; 75:307–15; PMID:23938317; http://dx.doi.org/10.1016/j.biopsych.2013.07.011
   PubMed Web of Science ®Google Scholar
• Meyer U. Developmental neuroinflammation and schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 2013; 42:20–34; PMID:22122877; http://dx.doi.org/10.1016/j.pnpbp.2011.11.003
   PubMed Web of Science ®Google Scholar
• Miller BJ, Culpepper N, Rapaport MH, Buckley P. Prenatal inflammation and neurodevelopment in schizophrenia: a review of human studies. Prog Neuropsychopharmacol Biol Psychiatry 2013; 42:92–100; PMID:22510462; http://dx.doi.org/10.1016/j.pnpbp.2012.03.010
   PubMed Web of Science ®Google Scholar
• Meyer U, Nyffeler M, Engler A, Urwyler A, Schedlowski M, Knuesel I, Yee BK, Feldon J. The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J Neurosci. 2006; 26:4752–62; PMID:16672647; http://dx.doi.org/10.1523/JNEUROSCI.0099-06.2006
   PubMed Web of Science ®Google Scholar
• Piontkewitz Y, Arad M, Weiner I. Abnormal trajectories of neurodevelopment and behavior following in utero insult in the rat. Biol Psychiatry 2011; 70:842–51; PMID:21816387; http://dx.doi.org/10.1016/j.biopsych.2011.06.007
   PubMed Web of Science ®Google Scholar
• Lister R, Mukamel EA, Nery JR, Urich M, Puddifoot CA, Johnson ND, Lucero J, Huang Y, Dwork AJ, Schultz MD, et al. Global epigenomic reconfiguration during mammalian brain development. Science 2013; 341:1237905; PMID:23828890; http://dx.doi.org/10.1126/science.1237905
   PubMed Web of Science ®Google Scholar
• Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003; 33Suppl:245–54; PMID:12610534; http://dx.doi.org/10.1038/ng1089
   PubMed Web of Science ®Google Scholar
• Connor CM, Dincer A, Straubhaar J, Galler JR, Houston IB, Akbarian S. Maternal immune activation alters behavior in adult offspring, with subtle changes in the cortical transcriptome and epigenome. Schizophr Res 2012; 140:175–84; PMID:22804924; http://dx.doi.org/10.1016/j.schres.2012.06.037
   PubMed Web of Science ®Google Scholar
• Tang B, Jia H, Kast RJ, Thomas EA. Epigenetic changes at gene promoters in response to immune activation in utero. Brain Behav Immun 2013; 30:168–75; PMID:23402795; http://dx.doi.org/10.1016/j.bbi.2013.01.086
   PubMed Web of Science ®Google Scholar
• Basil P, Li Q, Dempster EL, Mill J, Sham PC, Wong CC, McAlonan GM. Prenatal maternal immune activation causes epigenetic differences in adolescent mouse brain. Transl Psychiatry 2014; 4:e434; PMID:25180573; http://dx.doi.org/10.1038/tp.2014.80
   PubMed Web of Science ®Google Scholar
• Hollins SL, Zavitsanou K, Walker FR, Cairns MJ. Alteration of imprinted Dlk1-Dio3 miRNA cluster expression in the entorhinal cortex induced by maternal immune activation and adolescent cannabinoid exposure. Transl Psychiatry 2014; 4:e452; PMID:25268256; http://dx.doi.org/10.1038/tp.2014.99
   PubMed Web of Science ®Google Scholar
• Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 2005; 6:312–24; PMID:15803162; http://dx.doi.org/10.1038/nrn1648
   PubMed Web of Science ®Google Scholar
• Guidotti A, Auta J, Chen Y, Davis JM, Dong E, Gavin DP, Grayson DR, Matrisciano F, Pinna G, Satta R, et al. Epigenetic GABAergic targets in schizophrenia and bipolar disorder. Neuropharmacol 2011; 60:1007–16; PMID:21074545; http://dx.doi.org/10.1016/j.neuropharm.2010.10.021
   PubMed Web of Science ®Google Scholar
• Blatt GJ, Fatemi SH. Alterations in GABAergic biomarkers in the autism brain: research findings and clinical implications. Anat Rec 2011; 294:1646–5; http://dx.doi.org/10.1002/ar.21252
   Google Scholar
• Sibille E, Morris HM, Kota RS, Lewis DA. GABA-related transcripts in the dorsolateral prefrontal cortex in mood disorders. Int J Neuropsychopharmacol 2011; 14:721–34; PMID:21226980; http://dx.doi.org/10.1017/S1461145710001616
   PubMed Web of Science ®Google Scholar
• Akbarian S, Huang HS. Molecular and cellular mechanisms of altered GAD1/GAD67 expression in schizophrenia and related disorders. Brain Res Rev 2006; 52:293–304; PMID:16759710; http://dx.doi.org/10.1016/j.brainresrev.2006.04.001
   PubMed Web of Science ®Google Scholar
• Asada H, Kawamura Y, Maruyama K, Kume H, Ding RG, Kanbara N, Kuzume H, Sanbo M, Yagi T, Obata K. Cleft palate and decreased brain gamma-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci U S A 1997; 94:6496–9; PMID:9177246; http://dx.doi.org/10.1073/pnas.94.12.6496
   PubMed Web of Science ®Google Scholar
• Tian N, Petersen C, Kash S, Baekkeskov S, Copenhagen D, Nicoll R. The role of the synthetic enzyme GAD65 in the control of neuronal gamma-aminobutyric acid release. Proc Natl Acad Sci U S A 1999; 96:12911–6; PMID:10536022; http://dx.doi.org/10.1073/pnas.96.22.12911
   PubMed Web of Science ®Google Scholar
• Patel AB, de Graaf RA, Martin DL, Battaglioli G, Behar KL. Evidence that GAD65 mediates increased GABA synthesis during intense neuronal activity in vivo. J Neurochem 2006; 97:385–96; PMID:16539672; http://dx.doi.org/10.1111/j.1471-4159.2006.03741.x
   PubMed Web of Science ®Google Scholar
• Glausier JR, Kimoto S, Fish KN, Lewis DA. Lower glutamic acid decarboxylase 65-kDa isoform messenger RNA and protein levels in the prefrontal cortex in schizoaffective disorder but not schizophrenia. Biol Psychiatry 2015; 77:167–76; PMID:24993056; http://dx.doi.org/10.1016/j.biopsych.2014.05.010
   PubMed Web of Science ®Google Scholar
• Grayson DR, Guidotti A. The dynamics of DNA methylation in schizophrenia and related psychiatric disorders. Neuropsychopharmacology 2013; 38:138–166; PMID:22948975; http://dx.doi.org/10.1038/npp.2012.125
   PubMed Web of Science ®Google Scholar
• Zhubi A, Cook EH, Guidotti A, Grayson DR. Epigenetic mechanisms in autism spectrum disorder. Int Rev Neurobiol 2014; 115:203–44; PMID:25131546; http://dx.doi.org/10.1016/B978-0-12-801311-3.00006-8
   PubMed Web of Science ®Google Scholar
• Huang HS, Akbarian S. GAD1 mRNA expression and DNA methylation in prefrontal cortex of subjects with schizophrenia. PLoS One. 2007; 2:e809; PMID:17726539; http://dx.doi.org/10.1371/journal.pone.0000809
   PubMed Web of Science ®Google Scholar
• Dong E, Ruzicka WB, Grayson DR, Guidotti A. DNA-methyltransferase1 (DNMT1) binding to CpG rich GABAergic and BDNF promoters is increased in the brain of schizophrenia and bipolar disorder patients. Schizophr Res 2014; 167(1-3):35–41, in press; Epub ahead of print
   PubMed Web of Science ®Google Scholar
• Zhubi A, Chen Y, Dong E, Cook EH, Guidotti A, Grayson DR. Increased binding of MeCP2 to the GAD1 and RELN promoters may be mediated by an enrichment of 5-hmC in autism spectrum disorder (ASD) cerebellum. Transl Psychiatry 2014; 4:e349; PMID:24448211; http://dx.doi.org/10.1038/tp.2013.123
   PubMed Web of Science ®Google Scholar
• Dong E, Gavin DP, Chen Y, Davis J. Upregulation of TET1 and downregulation of APOBEC3A and APOBEC3C in the parietal cortex of psychotic patients. Transl Psychiatry 2012; 2:e159; PMID:22948384; http://dx.doi.org/10.1038/tp.2012.86
   PubMed Web of Science ®Google Scholar
• Gavin DP, Sharma RP, Chase KA, Matrisciano F, Dong E, Guidotti A. Growth arrest and DNA-damage-inducible, β (GADD45b)-mediated DNA demethylation in major psychosis. Neuropsychopharmacology 2012; 37:531–42; PMID:22048458; http://dx.doi.org/10.1038/npp.2011.221
   PubMed Web of Science ®Google Scholar
• Richetto J, Calabrese F, Riva MA, Meyer U. Prenatal immune activation induces maturation-dependent alterations in the prefrontal GABAergic transcriptome. Schizophr Bull 2014; 40:351–61; PMID:23328159; http://dx.doi.org/10.1093/schbul/sbs195
   PubMed Web of Science ®Google Scholar
• Richetto J, Labouesse MA, Poe MM, Cook JM, Grace AA, Riva MA, Meyer U. Behavioral effects of the benzodiazepine-positive allosteric modulator SH-053-2'F-S-CH₃ in an immune-mediated neurodevelopmental disruption model. Int J Neuropsychopharmacol 2015; 18(4); PMID:25636893; http://dx.doi.org/10.1093/ijnp/pyu055
   PubMed Web of Science ®Google Scholar
• Meyer U, Feldon J, Fatemi SH. In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci Biobehav Rev 2009; 33:1061–79; PMID:19442688; http://dx.doi.org/10.1016/j.neubiorev.2009.05.001
   PubMed Web of Science ®Google Scholar
• Richetto J, Calabrese F, Meyer U, Riva MA. Prenatal versus postnatal maternal factors in the development of infection-induced working memory impairments in mice. Brain Behav Immun 2013; 33:190–200; PMID:23876745; http://dx.doi.org/10.1016/j.bbi.2013.07.006
   PubMed Web of Science ®Google Scholar
• Malkova NV, Yu CZ, Hsiao EY, Moore MJ, Patterson PH. Maternal immune activation yields offspring displaying mouse versions of the three core symptoms of autism. Brain Behav Immun 2012; 26:607–16; PMID:22310922; http://dx.doi.org/10.1016/j.bbi.2012.01.011
   PubMed Web of Science ®Google Scholar
• Globisch D, Münzel M, Müller M, Michalakis S, Wagner M, Koch S, Brückl T, Biel M, Carell T. Tissue distribution of 5-hydroxymethylcytosine and search for active demethylation intermediates. PLoS One 2010; 5:e15367; PMID:21203455; http://dx.doi.org/10.1371/journal.pone.0015367
   PubMed Web of Science ®Google Scholar
• Jin SG, Wu X, Li AX, Pfeifer GP. Genomic mapping of 5-hydroxymethylcytosine in the human brain. Nucleic Acids Res 2011; 39:5015–24; PMID:21378125; http://dx.doi.org/10.1093/nar/gkr120
   PubMed Web of Science ®Google Scholar
• Guo X, Wu X, Ren L, Liu G, Li L. Emerging roles of TET proteins and 5-hydroxymethylcytosines in active DNA demethylation and beyond. Cell Cycle 2011; 10:2662–8; PMID:21811096; http://dx.doi.org/10.4161/cc.10.16.17093
   PubMed Web of Science ®Google Scholar
• Matrisciano F, Tueting P, Dalal I, Kadriu B, Grayson DR, Davis JM, Nicoletti F, Guidotti A. Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice. Neuropharmacology 2013; 68:184–94; PMID:22564440; http://dx.doi.org/10.1016/j.neuropharm.2012.04.013
   PubMed Web of Science ®Google Scholar
• Dong E, Dzitoyeva SG, Matrisciano F, Tueting P, Grayson DR, Guidotti A. Brain-derived neurotrophic factor epigenetic modifications associated with schizophrenia-like phenotype induced by prenatal stress in mice. Biol Psychiatry 2015; 77:589–96; PMID:25444166; http://dx.doi.org/10.1016/j.biopsych.2014.08.012
   PubMed Web of Science ®Google Scholar
• Zhang TY, Hellstrom IC, Bagot RC, Wen X, Diorio J, Meaney MJ. Maternal care and DNA methylation of a glutamic acid decarboxylase 1 promoter in rat hippocampus. J Neurosci 2010; 30:13130–7; PMID:20881131; http://dx.doi.org/10.1523/JNEUROSCI.1039-10.2010
   PubMed Web of Science ®Google Scholar
• Hyde TM, Lipska BK, Ali T, Mathew SV, Law AJ, Metitiri OE, Straub RE, Ye T, Colantuoni C, Herman MM, et al. Expression of GABA signaling molecules KCC2, NKCC1, and GAD1 in cortical development and schizophrenia. J Neurosci 2011; 31:11088–95; PMID:21795557; http://dx.doi.org/10.1523/JNEUROSCI.1234-11.2011
   PubMed Web of Science ®Google Scholar
• Catts VS, Fung SJ, Long LE, Joshi D, Vercammen A, Allen KM, Fillman SG, Rothmond DA, Sinclair D, Tiwari Y, et al. Rethinking schizophrenia in the context of normal neurodevelopment. Front Cell Neurosci. 2013; 7:60; PMID:23720610; http://dx.doi.org/10.3389/fncel.2013.00060
   PubMed Web of Science ®Google Scholar
• Takai D, Jones PA. Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc Natl Acad Sci U S A. 2002; 99:3740–5; PMID:11891299; http://dx.doi.org/10.1073/pnas.052410099
   PubMed Web of Science ®Google Scholar
• Kinde B, Gabel HW, Gilbert CS, Griffith EC, Greenberg ME. Reading the unique DNA methylation landscape of the brain: Non-CpG methylation, hydroxymethylation, and MeCP2. Proc Natl Acad Sci U S A 2015; 112:6800–6; PMID:25739960; http://dx.doi.org/10.1073/pnas.1411269112
   PubMed Web of Science ®Google Scholar
• Chao HT, Chen H, Samaco RC, Xue M, Chahrour M, Yoo J, Neul JL, Gong S, Lu HC, Heintz N, et al. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 2010; 468:263–9; PMID:21068835; http://dx.doi.org/10.1038/nature09582
   PubMed Web of Science ®Google Scholar
• Guy J, Cheval H, Selfridge J, Bird A. The role of MeCP2 in the brain. Annu Rev Cell Dev Biol 2011; 27:631–52; PMID:21721946; http://dx.doi.org/10.1146/annurev-cellbio-092910-154121
   PubMed Web of Science ®Google Scholar
• Chahrour M, Jung SY, Shaw C, Zhou X, Wong ST, Qin J, Zoghbi HY. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 2008; 320:1224–9; PMID:18511691; http://dx.doi.org/10.1126/science.1153252
   PubMed Web of Science ®Google Scholar
• Sugino K, Hempel CM, Okaty BW, Arnson HA, Kato S, Dani VS, Nelson SB. Cell-type-specific repression by methyl-CpG-binding protein 2 is biased toward long genes. J Neurosci 2014; 34:12877–83; PMID:25232122; http://dx.doi.org/10.1523/JNEUROSCI.2674-14.2014
   PubMed Web of Science ®Google Scholar
• He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, Ding J, Jia Y, Chen Z, Li L, et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 2011; 333:1303–7; PMID:21817016; http://dx.doi.org/10.1126/science.1210944
   PubMed Web of Science ®Google Scholar
• Kaas GA, Zhong C, Eason DE, Ross DL, Vachhani RV, Ming GL, King JR, Song H, Sweatt JD. TET1 controls CNS 5-methylcytosine hydroxylation, active DNA demethylation, gene transcription, and memory formation. Neuron 2013; 79:1086–93; PMID:24050399; http://dx.doi.org/10.1016/j.neuron.2013.08.032
   PubMed Web of Science ®Google Scholar
• Rudenko A, Dawlaty MM, Seo J, Cheng AW, Meng J, Le T, Faull KF, Jaenisch R, Tsai LH. Tet1 is critical for neuronal activity-regulated gene expression and memory extinction. Neuron 2013; 79:1109–22; PMID:24050401; http://dx.doi.org/10.1016/j.neuron.2013.08.003
   PubMed Web of Science ®Google Scholar
• Li X, Wei W, Zhao QY, Widagdo J, Baker-Andresen D, Flavell CR, D'Alessio A, Zhang Y, Bredy TW. Neocortical Tet3-mediated accumulation of 5-hydroxymethylcytosine promotes rapid behavioral adaptation. Proc Natl Acad Sci U S A 2014; 111:7120–5; PMID:24757058; http://dx.doi.org/10.1073/pnas.1318906111
   PubMed Web of Science ®Google Scholar
• Guidotti A, Grayson DR. DNA methylation and demethylation as targets for antipsychotic therapy. Dialogues Clin Neurosci 2014; 16:419–29; PMID:25364290
   PubMed Web of Science ®Google Scholar
• Braconi C, Huang N, Patel T. MicroRNA-dependent regulation of DNA methyltransferase-1 and tumor suppressor gene expression by interleukin-6 in human malignant cholangiocytes. Hepatology. 2010; 51:881–90; PMID:20146264
   PubMed Web of Science ®Google Scholar
• Foran E, Garrity-Park MM, Mureau C, Newell J, Smyrk TC, Limburg PJ, Egan LJ. Upregulation of DNA methyltransferase-mediated gene silencing, anchorage-independent growth, and migration of colon cancer cells by interleukin-6. Mol Cancer Res 2010; 8:471–81; PMID:20354000; http://dx.doi.org/10.1158/1541-7786.MCR-09-0496
   PubMed Web of Science ®Google Scholar
• Smith SE, Li J, Garbett K, Mirnics K, Patterson PH. Maternal immune activation alters fetal brain development through interleukin-6. J Neurosci 2007; 27:10695–702; PMID:17913903; http://dx.doi.org/10.1523/JNEUROSCI.2178-07.2007
   PubMed Web of Science ®Google Scholar
• Lipina TV, Zai C, Hlousek D, Roder JC, Wong AH. Maternal immune activation during gestation interacts with Disc1 point mutation to exacerbate schizophrenia-related behaviors in mice. J Neurosci 2013; 33:7654–66; PMID:23637159; http://dx.doi.org/10.1523/JNEUROSCI.0091-13.2013
   PubMed Web of Science ®Google Scholar
• Lam LL, Emberly E, Fraser HB, Neumann SM, Chen E, Miller GE, Kobor MS. Factors underlying variable DNA methylation in a human community cohort. Proc Natl Acad Sci U S A 2012; 109:17253–60; PMID:23045638; http://dx.doi.org/10.1073/pnas.1121249109
   PubMed Web of Science ®Google Scholar
• Klengel T, Binder EB. Epigenetics of Stress-Related Psychiatric Disorders and Gene × Environment Interactions. Neuron 2015; 86:1343–57; PMID:26087162; http://dx.doi.org/10.1016/j.neuron.2015.05.036
   PubMed Web of Science ®Google Scholar
• Szulwach KE, Li X, Li Y, Song CX, Wu H, Dai Q, Irier H, Upadhyay AK, Gearing M, Levey AI, et al. 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat Neurosci 2011; 14:1607–16; PMID:22037496; http://dx.doi.org/10.1038/nn.2959
   PubMed Web of Science ®Google Scholar
• Simmons RK, Stringfellow SA, Glover ME, Wagle AA, Clinton SM. DNA methylation markers in the postnatal developing rat brain. Brain Res 2013; 1533:26–36; PMID:23954679; http://dx.doi.org/10.1016/j.brainres.2013.08.005
   PubMed Web of Science ®Google Scholar
• Siegmund KD, Connor CM, Campan M, Long TI, Weisenberger DJ, Biniszkiewicz D, Jaenisch R, Laird PW, Akbarian S. DNA methylation in the human cerebral cortex is dynamically regulated throughout the life span and involves differentiated neurons. PLoS One 2007; 2:e895; PMID:17878930; http://dx.doi.org/10.1371/journal.pone.0000895
   PubMed Web of Science ®Google Scholar
• Fabbri M, Garzon R, Cimmino A, Liu Z, Zanesi N, Callegari E, Liu S, Alder H, Costinean S, Fernandez-Cymering C, et al. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A 2007; 104:15805–10; PMID:17890317; http://dx.doi.org/10.1073/pnas.0707628104
   PubMed Web of Science ®Google Scholar
• Miller BH, Zeier Z, Xi L, Lanz TA, Deng S, Strathmann J, Willoughby D, Kenny PJ, Elsworth JD, Lawrence MS, et al. MicroRNA-132 dysregulation in schizophrenia has implications for both neurodevelopment and adult brain function. Proc Natl Acad Sci U S A 2012; 109:3125–30; PMID:22315408; http://dx.doi.org/10.1073/pnas.1113793109
   PubMed Web of Science ®Google Scholar
• Mellios N, Sugihara H, Castro J, Banerjee A, Le C, Kumar A, Crawford B, Strathmann J, Tropea D, Levine SS, et al. miR-132, an experience-dependent microRNA, is essential for visual cortex plasticity. Nat Neurosci 2011; 14:1240–2; PMID:21892155; http://dx.doi.org/10.1038/nn.2909
   PubMed Web of Science ®Google Scholar
• Shaked I, Meerson A, Wolf Y, Avni R, Greenberg D, Gilboa-Geffen A, Soreq H. MicroRNA-132 potentiates cholinergic anti-inflammatory signaling by targeting acetylcholinesterase. Immunity 2009; 31:965–73; PMID:20005135; http://dx.doi.org/10.1016/j.immuni.2009.09.019
   PubMed Web of Science ®Google Scholar
• Fujihara K, Miwa H, Kakizaki T, Kaneko R, Mikuni M, Tanahira C, Tamamaki N, Yanagawa Y. Glutamate decarboxylase 67 deficiency in a subset of GABAergic neurons induces schizophrenia-related phenotypes. Neuropsychopharmacology 2015; 40(10):2475–86, in press; [ Epub ahead of print]
   PubMed Web of Science ®Google Scholar
• Mitchell AC, Jiang Y, Peter C, Akbarian S. Transcriptional regulation of GAD1 GABA synthesis gene in the prefrontal cortex of subjects with schizophrenia. Schizophr Res 2015; 167(1-3):28–34, in press; [ Epub ahead of print]
   PubMed Web of Science ®Google Scholar
• Gapp K, Woldemichael BT, Bohacek J, Mansuy IM. Epigenetic regulation in neurodevelopment and neurodegenerative diseases. Neuroscience 2014; 264:99–111; PMID:23256926; http://dx.doi.org/10.1016/j.neuroscience.2012.11.040
   PubMed Web of Science ®Google Scholar
• Sweatt JD. Experience-dependent epigenetic modifications in the central nervous system. Biol Psychiatry 2009; 65:191–7; PMID:19006788; http://dx.doi.org/10.1016/j.biopsych.2008.09.002
   PubMed Web of Science ®Google Scholar
• Roadmap Epigenomics Consortium. Integrative analysis of 111 reference human epigenomes. Nature 2015; 518:317–30; PMID:25693563; http://dx.doi.org/10.1038/nature14248
   PubMed Web of Science ®Google Scholar
• Sims RJ, 3rd, Nishioka K, Reinberg D. Histone lysine methylation: a signature for chromatin function. Trends Genet 2003; 19:629–39; PMID:14585615; http://dx.doi.org/10.1016/j.tig.2003.09.007
   PubMed Web of Science ®Google Scholar
• Tremolizzo L, Doueiri MS, Dong E, Grayson DR, Davis J, Pinna G, Tueting P, Rodriguez-Menendez V, Costa E, Guidotti A. Valproate corrects the schizophrenia-like epigenetic behavioral modifications induced by methionine in mice. Biol Psychiatry 2005; 57:500–9; PMID:15737665; http://dx.doi.org/10.1016/j.biopsych.2004.11.046
   PubMed Web of Science ®Google Scholar
• Dong E, Agis-Balboa RC, Simonini MV, Grayson DR, Costa E, Guidotti A. Reelin and glutamic acid decarboxylase67 promoter remodeling in an epigenetic methionine-induced mouse model of schizophrenia. Proc Natl Acad Sci U S A 2005; 102:12578–83; PMID:16113080; http://dx.doi.org/10.1073/pnas.0505394102
   PubMed Web of Science ®Google Scholar
• Dong E, Guidotti A, Grayson DR, Costa E. Histone hyperacetylation induces demethylation of reelin and 67-kDa glutamic acid decarboxylase promoters. Proc Natl Acad Sci U S A 2007; 104:4676–81; PMID:17360583; http://dx.doi.org/10.1073/pnas.0700529104
   PubMed Web of Science ®Google Scholar
• Kundakovic M, Chen Y, Costa E, Grayson DR. DNA methyltransferase inhibitors coordinately induce expression of the human reelin and glutamic acid decarboxylase 67 genes. Mol Pharmacol 2007; 71:644–53; PMID:17065238; http://dx.doi.org/10.1124/mol.106.030635
   PubMed Web of Science ®Google Scholar
• Kundakovic M, Chen Y, Guidotti A, Grayson DR. The reelin and GAD67 promoters are activated by epigenetic drugs that facilitate the disruption of local repressor complexes. Mol Pharmacol 2009; 75:342–54; PMID:19029285; http://dx.doi.org/10.1124/mol.108.051763
   PubMed Web of Science ®Google Scholar
• Meyer U, Knuesel I, Nyffeler M, Feldon J. Chronic clozapine treatment improves prenatal infection-induced working memory deficits without influencing adult hippocampal neurogenesis. Psychopharmacology 2010; 208:531–43; PMID:20041229; http://dx.doi.org/10.1007/s00213-009-1754-6
   PubMed Web of Science ®Google Scholar
• Dong E, Nelson M, Grayson DR, Costa E, Guidotti A. Clozapine and sulpiride but not haloperidol or olanzapine activate brain DNA demethylation. Proc Natl Acad Sci U S A 2008; 105:13614–9; PMID:18757738; http://dx.doi.org/10.1073/pnas.0805493105
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25:402–8; PMID:11846609; http://dx.doi.org/10.1006/meth.2001.1262
   PubMed Web of Science ®Google Scholar